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Surgical and Radiologic Anatomy

https://doi.org/10.1007/s00276-018-1977-5

ORIGINAL ARTICLE

Anatomical and histological study of the deep neck fasciae: does


the alar fascia exist?
M. Gavid1,2   · J. M. Dumollard3 · C. Habougit3 · Y. Lelonge2 · F. Bergandi1 · M. Peoc’h3 · J. M. Prades1,2

Received: 10 October 2017 / Accepted: 18 January 2018


© Springer-Verlag France SAS, part of Springer Nature 2018

Abstract
Purpose  The aim of this study was to determine whether the alar fascia is a distinct layer of the deep cervical neck fasciae.
The present study also aimed to elucidate the anatomical limits of this fascia.
Methods  Neck dissections of ten adult cadavers were performed, layer by layer, in the retropharyngeal region, under a
powered operating microscope. Detailed dissections revealed the anatomical limits of the deep neck fasciae. Histological
descriptions were also performed on large tissue samples collected from three cervical dissections.
Results  In the ten dissections, three layers of fascia were identified and dissected in the retropharyngeal region: a visceral
fascia, a prevertebral fascia and an alar fascia. The alar fascia appeared like a connecting band derivative of the visceral
fascia, between both vascular sheaths. It fused completely with the visceral fascia anteriorly at the level of T2 and with the
prevertebral fascia posteriorly at the level of C1. No sagittal connection between the visceral fascia and the prevertebral
fascia was identified. The stained histological sections confirmed the presence of the visceral and prevertebral fasciae at the
oropharyngeal level, with a third intermediate layer closely connected with the visceral fascia.
Conclusion  The alar fascia is a layer of the cervical neck fascia connected with the visceral fascia from C1 to T2 levels.
The anatomical limits of this alar fascia and its relationships with the internal carotid artery are important in the surgical
management and the prognosis of deep neck infections and retropharyngeal lymph node metastases.

Keywords  Alar fascia · Visceral fascia · Prevertebral fascia · Layer of the cervical fascia · Retropharyngeal node

Introduction The middle layer is considered as made up of three divi-


sions: the sternohyoid-omohyoid layer, the sternothyroid-
The deep fasciae of the head and neck have been a subject of thyrohyoid layer and the visceral fascia [20]. This visceral
controversy for many years to such an extent that Malgaigne fascia has also been described under different names such as
stated that: “The cervical fasciae appear in a new form under the pretracheal or buccopharyngeal fascia.
the pen of each author who attempts to describe them” [14]. Descriptions of the deep layer of the deep cervical fas-
In 1882, Tillaux was the first to describe three layers of cia are the most controversial. In literature, most investi-
the deep cervical fasciae (CF): the superficial, the middle gators usually described the deep layer as the prevertebral
and the deep layer [25]. Since that time, this description has layer [20–22, 24], though, an additional layer between the
been generally used and confirmed [20, 22, 24]. visceral and the prevertebral fascia, named the alar fascia,
was described by Grodinsky in 1939 [9]. The existence of
this alar fascia is still a controversial point. Indeed, a simple
* M. Gavid look at teaching anatomical textbooks is a good illustration
marie.gavid@chu‑st‑etienne.fr of this controversy: no alar fascia is drawn nor described
in Kamina’s teaching book [12], whereas Gray’s teaching
1
Department of Anatomy, Jean Monnet University, book of anatomy mentions the alar fascia as an inconstant
Saint‑Etienne, France
fascia [13].
2
Department of Otorhinolaryngology Head Neck Surgery, The aim of this study was to investigate whether the alar
CHU Saint-Etienne, Saint‑Etienne, France
fascia exists. We also performed an anatomical description
3
Department of Anatomopathology, CHU Saint-Etienne, of the alar fascia focusing on its limits and its relationship
Saint‑Etienne, France

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Surgical and Radiologic Anatomy

to the carotid sheath, the visceral fascia and the prevertebral


fascia.

Materials and methods

The cervical region of ten fresh adult human cadavers (seven


males, three females) provided by the division of Anatomy
at Saint-Etienne Medical School were dissected. Neck dis-
sections were performed layer-by-layer and examined under
a Wild Leitz Heerburg microscope. Visceral track was first
detected, dissected and preserved. The anatomical structures
such as carotid artery and vascular sheath were also identi-
fied and preserved. Then the different layers of fascia were
identified and dissected anteriorly to posteriorly. Special Fig. 1  The retropharyngeal fasciae: the visceral fascia, the alar fascia
and the prevertebral fascia (M×15). Asterisk indicates the preverte-
attention was paid to the anatomical limits of these neck bral fascia. Open triangle indicates the alar fascia. Currency sign indi-
fasciae. cates the visceral fascia
Over the ten cervical dissections, three were dissected to
isolate the pharynx and the retropharyngeal tissues. Large
samples of tissue were collected and underwent fixation in
10% buffered formalin followed by paraffin embedding. His-
tological sections from paraffin-embedded blocks were rou-
tinely stained with haematoxylin, eosin and saffron (HES),
and secondarily with Masson’s trichrome. The sectional
planes were horizontal. A sample was collected in each dis-
section at the level of the inferior limit of the oropharynx. In
the first sample, dissection collected a tissue block contain-
ing pharyngeal mucosa, retropharyngeal tissues and mus-
cles up to prevertebral muscle. The two other samples just
contained the pharyngeal mucosa and the retropharyngeal
tissues in front of the prevertebral fascia. No prevertebral
fascia and muscles were collected in order to preserve the
quality of the alar fascia tissue.
Fig. 2  The alar fascia: connecting band between both vascular sheath,
cotton within the nasopharyngeal space (M×6). Asterisk indicates the
Results carotid artery. Down arrow indicates the alar fascia. Closed triangle
indicates the visceral tract surrounded by the visceral fascia
Anatomical findings

Similar observational patterns were identified in all cadav- dissection did not give enough details to determine the exact
ers’ dissection. In the ten dissections, three layers of fascia relationship between those two fasciae. Histological exami-
were identified and dissected anteriorly to posteriorly: a vis- nation was necessary.
ceral fascia, an alar fascia and a prevertebral fascia (Fig. 1). The dissected alar fascia extended posterior to the visceral
The visceral fascia which belongs to the middle layer fascia across the midline on both sides. It fused laterally with
of the CF was identified encircling the trachea, the thyroid the vascular sheath and contributed to the medial walls of
gland, the pharynx and the oesophagus. Posteriorly, the pre- the vascular sheath (Figs. 2, 3). No connection with the tip
vertebral fascia (deep layer of the CF) adhered directly to the of the transverse process was identified. The superior and
vertebral column and the cervical muscles. inferior limits of the alar fascia were less distinct. No sagit-
The alar fascia was identified as a connecting band tal connections between the visceral and the prevertebral
between both vascular sheaths (Fig. 2). It was closely linked fasciae were identified. Superiorly the alar fascia could not
to the visceral fascia to such an extent that it appeared mac- be dissected from the prevertebral fascia. It fused with the
roscopically as a thin layer developed at the expanse of the prevertebral fascia regarding C1. No distinct alar fascia was
visceral fascia. The powered operating microscope used for identified superior to C1 in all dissections. The alar fascia

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Surgical and Radiologic Anatomy

Fig. 3  The alar fascia through neck dissection: its superior and infe-
rior limits (M×6). Open triangle indicates the alar fascia. Open left
arrow indicates the visceral tract surrounded by the visceral fascia. Fig. 5  Horizontal section at the level of the oropharynx. Masson’s
Asterisk indicates the carotid artery Trichrome stain. 1: The visceral fascia. 2: The alar fascia. 3: The pre-
vertebral fascia, open down arrow indicates the alar fascia. A: The
oropharyngeal mucosa. B: The superior constrictor muscle of the
pharynx. C: The prevertebral muscles

Fig. 4  Diagram of the three retropharyngeal layers of fascia and the


two deep neck spaces. 1: The visceral fascia. 2: The alar fascia. 3:
The prevertebral fascia. A: The retropharyngeal space. B: The danger
space

could be dissected until T2 in every dissection. Inferiorly,


the alar fascia fused progressively and completely with the
visceral fascia, between T2 and T4. The alar fascia divided
the space between the pharynx and the vertebra into two
compartments: the retropharyngeal compartment anteriorly
and the danger space posteriorly (Fig. 4).

Histological findings

Figures 5 shows histological section stained by Masson’s Fig. 6  Horizontal sections at the level of the oropharynx. HES stain.
trichrome. Between the prevertebral muscles and the con- 1: The visceral fascia. 2: The alar fascia. Asterisk indicates the
strictor muscle of the pharynx, three layers of fascia were merger between the visceral fascia and the alar fascia. Up arrow indi-
cates the alar fascia. A: The oropharyngeal mucosa. B: The superior
identified. The Masson’s Trichrome staining highlighted the constrictor muscle of the pharynx. Currency sign indicates the carotid
collagen fibers of these three layers. In Fig. 6, the distinc- artery
tion between the alar fascia and the visceral fascia in less
evident. Indeed, the alar fascia appears as a layer medially
merged with the visceral fascia. Laterally, it contributes to Discussion
the medial and anterior wall of the carotid sheath. No con-
nection between the alar and the prevertebral fascia was This investigation aimed at defining the existence of the
identified in these oropharyngeal sections. No lymph nodes alar fascia in the cervical region using anatomical dissec-
or vessels were identified in these sections. tion and histological investigation.

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Surgical and Radiologic Anatomy

In literature, anatomy of cervical fasciae is still a matter merger between the two layers might explain the confusion
of debate, especially regarding the description of the layers over the existence of the alar fascia in literature.
of the deep cervical fascia [5, 13, 19]. Another source of discrepancy in literature is the ana-
The deep cervical fasciae have been divided into three tomical limits of the alar fascia. For Grodinsky, the alar
different layers by Tillaux in 1882 [25]: the superficial, fascia extended from the base of the skull to the seventh
the middle and the deep layer. Since then, many authors cervical vertebrae [9]. According to Vieira in 2008, the deep
have focused on the deep layer of the cervical fasciae. layer of the deep fascia splits into two layers as it reaches
For Charpy, in 1901, the deep layer of the cervical fascia the longus colli muscle: the alar and the prevertebral layer
corresponded to the prevertebral fascia [20]. But he also [27]. Using sheet plastination, Scali et al. pointed out that
described a sagittal connection between the prevertebral the alar fascia could not be identified above the level of C1:
and the visceral fascia, commonly known as “Charpy’s the superior limit of the alar fascia was the horizontal plane
sagittal connection”. Not only Testut in 1902 [24] and passing through the superior limit of the posterior tubercle
Rouvière [22] in 1927 referred to this description but also of the atlas [23]. In this study, the alar fascia could easily be
more contemporary literature such as Wong in 1978 [28] identified from C1 to T2. Above the level of C1 and under
and Chevrel in 1996 [5]. the level of T2, the alar fascia fused progressively with the
Grodinsky in 1939 revealed a different disposition of the prevertebral fascia superiorly and with the visceral fascia
deep layer of the cervical fascia [9]. In his study, the alar inferiorly. The absence of alar fascia under the level of T4 is
fascia was described as a complete layer of fascia between supported by embryological findings. Miyake’s work on late
the visceral and the prevertebral fasciae. It formed the fetuses (25 weeks) indicated connections between the alar
medio-anterior wall of the carotid sheath and fused with fascia and sheaths of the mediastinal great vessels [15]. The
the prevertebral fascia at the tip of the transverse process. multiple mergers of the alar fascia with the visceral fascia
This description was relayed and supported by different and the variability of the anatomical limits of the alar fascia
studies and reference books of anatomy [2, 11, 17, 19]. The might also explain the variety of results in literature regard-
alar fascia was also identified in a fetal anatomical study on ing existence of the alar fascia.
15–25 week fetuses [15]. It was described as a connecting Moreover, standard radiological examinations such as
band between both vascular sheaths. CT or MRI in normal individuals are unable to differentiate
Still, classical and contemporary reports remain incon- the alar fascia as a separate layer [6]. It can occasionally be
sistent regarding the existence of the alar fascia. As a con- identified in oedematous patients with post-radiation therapy
sequence, some commonly used anatomical textbooks con- [16]. Even if the alar fascia cannot be identified through
cluded that this alar fascia was an inconsistent layer of the normal radiology, its existence and anatomical limits must
prevertebral fascia [13]. be familiar to radiologists and surgeons for pathological rea-
In this study, a layer corresponding to the description of sons. Indeed, in deep neck infection, prognosis depends on
the alar fascia was identified in all cadaveric dissections. It whether the alar fascia has been crossed by the infection
was connected with both vascular sheaths as it contributed and the danger space has been contaminated. The danger
to their antero-medial wall. It appeared as a very thin layer space widely communicates with the entire posterior medi-
developed at the expanse of the visceral fascia. This fascia astinum. So, the danger lies in the possibility for infections
was highly connected to the visceral fascia and seemed to of the danger space to spread inferiorly into all the medi-
diverge from this fascia to contribute to the carotid sheath. astinum, resulting in complications such as mediastinitis,
It divided the space between the pharynx and the vertebra severe sepsis, pleural and pericardial effusions [27]. The
into two compartments: the retropharyngeal compartment mortality rate among adults is still 25% even with the use of
anteriorly and the danger space posteriorly. The histological broad-spectrum antibiotics [7]. As a consequence, infection
sections and staining achieved on three of the human cadaver crossing the alar fascia from the pharynx and spreading into
dissections also confirmed the existence of the alar fascia as the danger space must be diagnosed by radiologist so that
an expanse of the visceral fascia. Indeed, the visceral and thoracic diffusion will be investigated and taken into account
the alar fasciae were partially merged. The alar fascia had to decide whether mediastinal surgery is necessary.
a looser fibroareolar structure compared to the prevertebral On the contrary, retropharyngeal space infections con-
fascia. To the best of our knowledge, this is the first study fined in front of the alar fascia will not disseminate easily
in literature which describes histological aspects of this fas- through the entire mediastinum [27]. Indeed, the anterior
cia. The only other histological findings in literature were fusion between the alar fascia and the visceral fascia around
described in a fetal anatomical study by Miyake et al. [15]. the level of T2–T4 prevents infection from easily reach-
In 18 weeks fetuses, Miyake noticed that the visceral fascia ing the pericardial tissues. Source of infection of the ret-
“appeared to correspond to parts of the alar fascia”. The ropharyngeal space and the danger space is also different: the
infection of the danger space usually results from a traumatic

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Surgical and Radiologic Anatomy

penetration [7], whereas the infection of the retropharyngeal of deep neck infections. The close relationships of the alar
space usually reaches this space via the lymphatics most fascia with the vascular sheath and as a consequence with
commonly as a complication of suppurative tonsillitis, in the carotid artery are challenging in the surgical manage-
young children [3]. The retropharyngeal space contains on ment of retropharyngeal lymph node metastases.
each side two chains of lymph nodes lying medial to the
internal carotid artery at the level of the transverse process: Author contributions  MG: protocol/project development, data collec-
tion, manuscript writing. JMD: data analysis, manuscript writing. CH:
the medial and the lateral groups [22]. The medial group data analysis, histological figure management. YL: data analysis. FB:
of nodes is located anterior to the medial part of the longus data collection, dissection. MP: data analysis. JMP: protocol/project
colli muscles. The lateral group, also known as the nodes development, manuscript correction.
of Rouvière, lies ventral to the longus colli muscles. The
retropharyngeal nodes receive drainage from the nose, the Compliance with ethical standards 
nasopharynx, the oropharynx and the hypopharynx [4, 8].
Retropharyngeal nodes are normally present in children and Conflict of interest  The authors declare that they have no conflict of
interest.
then atrophy in puberty [18]. As a consequence, unilateral
retropharyngeal abcesses are primarily seen in childhood as
a complication of nasopharyngitis [7]. These abcesses do not
systematically spread into the mediastinum: mediastinitis
occurs in 1–24% [1, 10]. This clinical finding correlates well
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